Network synchrony of GABAergic interneurons in the intact hippocampus: Role of electrotonic coupling.

摘要

Rhythmic population neuronal activities of various frequencies have been observed in the hipocampus in vivo. Hippocampal interneurons play a crucial role in these neuronal population oscillations. This work investigates the properties of O/A interneurons and their interaction with emphasis on the synchronizing role of gap junctions. All experiments were performed in the isolated whole hippocampus preparation in which local neuronal circuits are intact and spontaneously rhythmic activities with peak frequencies ranging from 0.3 to 4 Hz are apparent. O/A interneurons manifested spontaneous polyphasic EPSPs which were highly synchronized between O/A interneurons and closely phase-related to the spontaneous rhythmic field potentials recorded in the nearby pyramidal CA1 region. Although common glutamatergic drive and mutual inhibition played a critical role in maintaining the spontaneous synchronized polyphasic EPSPs in O/A interneurons, gap junctional communication was also essential. Indeed, 10.6% of dual whole cell recordings in O/A interneurons in the present study showed direct electrotonic coupling. This coupling might mostly occur in distal dendrites because of the generally small coupling coefficient (6.9 ± 4.7%, range: 1.3 to 17.6%) and was intermittent. However, spikes in one of the coupled neurons were associated with small electrotonic EPSPs (spikelets) in those neuron pairs with coupling coefficients greater than 10%. Although the coupling rate estimated from dual whole cell recording was less than 10%, electrotonic coupling between O/A interneurons was much more extensive when scrutinizing individual whole cell recordings. In about 60% of recorded O/A interneurons, spontaneous postsynaptic potentials (PSPs) were apparent, and 20–30% of these PSPs were sensitive to gap junctional blockers. Moreover, the slow (12 Hz) baseline membrane potential oscillations of O/A interneurons were also markedly significantly affected by gap junctional blockers. These experimental results indicate that gap junctions link O/A interneurons extensively and play a vigorous and significant role in conducting and synchronizing electric signals between them.